Resveratrol derivative production by high-pressure treatment: proliferative inhibitory effects on cervical cancer cells

  • Yuki Sugahara Graduate School of Integrated Pharmaceutical and Nutrition Sciences, University of Shizuoka, Shizuoka, Japan
  • Toshiro Ohta Graduate School of Integrated Pharmaceutical and Nutrition Sciences, University of Shizuoka, Shizuoka, Japan
  • Yoshiki Taguchi Graduate School of Integrated Pharmaceutical and Nutrition Sciences, University of Shizuoka, Shizuoka, Japan
  • Sari Honda Graduate School of Integrated Pharmaceutical and Nutrition Sciences, University of Shizuoka, Shizuoka, Japan
  • Yasuhiro Kashima UHA Mikakuto Co., Ltd., Osaka, Japan
  • Taiji Matsukawa UHA Mikakuto Co., Ltd., Osaka, Japan
  • Shigenori Kumazawa Graduate School of Integrated Pharmaceutical and Nutrition Sciences, University of Shizuoka, Shizuoka, Japan
  • Wataru Kadowaki Graduate School of Integrated Pharmaceutical and Nutrition Sciences, University of Shizuoka, Shizuoka, Japan
Keywords: Food processing; Caffeic acid; Apoptosis; HeLa; PARP; p38

Abstract

Background: In recent years, functional food components have attracted considerable attention. Resveratrol, a food polyphenol, has been widely studied due to its various physiological activities. Previously, we identified a novel resveratrol derivative, named RK4, in food, which is formed by a chemical reaction involving resveratrol and caffeic acid. Furthermore, it was suggested that high-pressure treatment is an important factor in RK4 production.

Objectives: The purpose of this study was to clarify relationships between high-pressure processing and component production and to compare RK4 with the known functional ingredient resveratrol to examine the physiological value of RK4. Through this research, we aimed to develop high-pressure treatment technology that adds new usefulness for food.

Methods: Resveratrol and caffeic acid were reacted under high-pressure treatment and in various conditions of concentration and temperature. RK4 levels in the reaction solution were quantitatively analyzed using liquid chromatography-mass spectrometry. In addition, HeLa cervical cancer cells were exposed to RK4 and resveratrol, and survival rates were measured using the methyl thiazolyl tetrazolium (MTT) method after culturing for 24 h. Activation of an apoptosis-inducing marker was detected by western blotting of cells cultured for 48 h after addition of the test compounds.

Results: By reacting resveratrol and caffeic acid under high-pressure conditions (~100 MPa), the amount of RK4 produced was significantly increased. It was also found that the reaction temperature and time contributed to this reaction. RK4 exhibited stronger cytotoxicity to HeLa cells than resveratrol. It was also shown that RK4 activated p38, cleaved poly ADP ribose polymerase, and induced apoptosis.

Conclusions: RK4 is a valuable component for further research as a novel compound with wider functionality than that of resveratrol. High-pressure treatment may substantially contribute to the production of novel food ingredients. Further elucidation of the relationships between high-pressure treatment and production of new ingredients has promising potential to guide development of new applications in food processing.

Downloads

Download data is not yet available.

References


  1. Yamada T, Hayasaka S, Shibata Y, Ojima T, Saegusa T, Gotoh T, et al. Frequency of citrus fruit intake is associated with the incidence of cardiovascular disease: the Jichi Medical School cohort study. J Epidemiol 2011; 21: 169–75. doi: 10.2188/jea.JE20100084

  2. Mursu J, Virtanen JK, Tuomainen TP, Nurmi T, Voutilainen S. Intake of fruit, berries, and vegetables and risk of type 2 diabetes in Finnish men: the kuopio ischaemic heart disease risk factor study. Am J Clin Nutr 2014; 9: 328–33. doi: 10.3945/ajcn.113.069641

  3. Kruk J. Association between vegetable, fruit and carbohydrate intake and breast cancer risk in relation to physical activity. Asian Pac J Cancer Prev 2014; 15: 4429–36. doi: 10.7314/APJCP.2014.15.11.4429

  4. Kyro C, Skeie G, Loft S, Landberg R,Christensen J, Lund E, et al. Intake of whole grains from different cereal and food sources and incidence of colorectal cancer in the Scandinavian HELGA cohort. Cancer Causes Control 2013; 24: 1363–74. doi: 10.1007/s10552-013-0215-z

  5. Wang LF, Chen JY, Xie HH, Ju XR, Liu RH. Phytochemical profiles and antioxidant activity of adlay varieties. J Agric Food Chem 2013; 61: 5103–13. doi: 10.1021/jf400556s

  6. Prahalathan P, Saravanakumar M, Raja B. The flavonoid morin restores blood pressure and lipid metabolism in DOCA-salt hypertensive rats. Redox Rep 2012; 17: 167–75. doi: 10.1179/1351000212Y.0000000015

  7. St Leger AS, Cochrane A, Moore F. Factors associated with cardiac mortality in developed countries with particular reference to the consumption of wine. Lancet 1979; 313: 1017–20. doi: 10.1016/S0140-6736(79)92765-X

  8. Renaud S, De Lorgeril M. Wine, alcohol, platelets, and the French paradox for coronary heart disease. Lancet 1992; 339: 1523–6. doi: 10.1016/0140-6736(92)91277-F

  9. Frankel EN, Waterhouse AL, Kinsella JE. Inhibition of human LDL oxidation by resveratrol. Lancet 1993; 341: 1103–4. doi: 10.1016/0140-6736(93)92472-6

  10. Shukla Y, Singh R. Resveratrol and cellular mechanisms of cancer prevention. Ann NY Acad Sci 2011; 1215: 1–8. doi: 10.1111/j.1749-6632.2010.05870.x

  11. Malaguarnera L. Influence of resveratrol on the immune response. Nutrients 2019; 11: 946. doi: 10.3390/nu11050946

  12. Li H, Xia N, Hasselwander S, Daiber A. Resveratrol and vascular function. Int J Mol Sci 2019; 20: 2155. doi: 10.3390/ijms20092155

  13. Park SJ, Ahmad F, Philp A, Baar K, Williams T, Luo H, et al. Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting camp phosphodiesterases. Cell 2012; 148: 421–33. doi: 10.1016/j.cell.2012.01.017

  14. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, et al. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 2014; 19: 191–6. doi: 10.1038/nature01960

  15. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 2006; 444: 337–42. doi: 10.1038/nature05354

  16. Timmers S, Konings E, Bilet L, Houtkooper RH, Van De Weijer T, Goossens GH, et al. Calorie restriction-like effects of 30 days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans. Cell Metab 2011; 14: 612–22. doi: 10.1016/j.cmet.2011.10.002

  17. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating sirt1 and Pgc-1α. Cell 2006; 127: 1109–22. doi: 10.1016/j.cell.2006.11.013

  18. Kishi A, Shinka Y, Matsukawa T, Yamada Y, Yamada I. A novel resveratrol derivative. Japan Patent 2016; 30739.

  19. Okamoto H, Matsukawa T, Doi S, Tsunoda T, Sawata Y, Naemura M, et al. A novel resveratrol derivative selectively inhibits the proliferation of colorectal cancer cells with KRAS mutation. Mol Cell Biochem 2018; 442: 39–45. doi: 10.1007/s11010-017-3191-x

  20. Shimada A, Kasai M, Yamamoto A, Hatae K. Changes in the palatability of foods by hydrostatic pressurizing. Nippon Shokuhin Kogyo Gakkaishi (in Japanese) 1990; 37: 511–19. doi: 10.3136/nskkk1962.37.7_511

  21. Signorelli P, Ghidoni R. Resveratrol as an anticancer nutrient: molecular basis, open questions and promises. J Nutr Biochem 2005; 16: 449–66. doi: 10.1016/j.jnutbio.2005.01.017

  22. Carrizzo A, Forte M, Damato A, Trimarco V, Salzano F, Bartolo M, et al. Antioxidant effects of resveratrol in cardiovascular, cerebral and metabolic diseases. Food Chem Toxicol 2013; 61: 215–26. doi: 10.1016/j.fct.2013.07.021

  23. Jang M, Cai L, Udeani GO, Slowing KV, Thomas CF, Beecher CW, et al. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 1997; 275: 218–20. doi: 10.1126/science.275.5297.218

  24. Fouad MA, Agha AM, Merzabani MM, Shouman SA. Resveratrol inhibits proliferation, angiogenesis and induces apoptosis in colon cancer cells: calorie restriction is the force to the cytotoxicity. Hum Exp Toxicol 2013; 32: 1067–80. doi: 10.1177/0960327113475679

  25. Carter LG, D’Orazio JA, Pearson KJ. Resveratrol and cancer: focus on in vivo evidence. Endocr Relat Cancer 2014; 21: R209–25. doi: 10.1530/ERC-13-0171

  26. Li L, Qiu RL, Lin Y, Cai Y, Bian Y, Fan Y, et al. Resveratrol suppresses human cervical carcinoma cell proliferation and elevates apoptosis via the mitochondrial and p53 signaling pathways. Oncol Lett 2018; 15: 9845–51. doi: 10.3892/ol.2018.8571

  27. Zhang L, Yang X, Li X, Li C, Zhao L, Zhou Y, et al. Butein sensitizes HeLa cells to cisplatin through the AKT and ERK/p38 MAPK pathways by targeting FoxO3a. Int J Mol Med 2015; 36: 957–66. doi: 10.3892/ijmm.2015.2324

  28. Liu Z, Wu X, Lv J, Sun H, Zhou F. Resveratrol induces p53 in colorectal cancer through SET7/9. Oncol Lett 2019; 17: 3783–9. doi: 10.3892/ol.2019.10034

  29. Cohen GM. Caspases: the executioners of apoptosis. Biochem J 1997; 326: 1–16. doi: 10.1042/bj3260001

  30. Gorczyca W, Gong J, Ardelt B, Traganos F, Darzynklewiez Z. The cell cycle-related differences in susceptibility of HL-60 cells to apoptosis induced by various antitumor agents. Cancer Res 1993; 53: 3186–92.

  31. Xiao D, Zhu SP, Gu ZL. Quercetin induced apoptosis in human leukemia HL-60 cell. Acta Pharmacol Sinica 1998; 18: 280–3.

  32. Yin F, Giuliano AE, Van Herle AJ. Signal pathways involved in apigenin inhibition of growth and induction of apoptosis of human anaplastic thyroid cancer cells (ARO). Anticancer Res 1999; 19: 4297–303.

  33. Hsu FL, Chen YC, Cheng JT. Caffeic acid as active principle from the fruit of Xanthium strumarium to lower plasma glucose in diabetic rats. Planta Med 2000; 66: 228–30. doi: 10.1055/s-2000-8561

  34. Giovannini L, Migliori M, Filippi C, Origlia N, Panichi V, Falchi M, et al. Inhibitory activity of the white wine compounds, tyrosol and caffeic acid, on lipopolysaccharide-induced tumor necrosis factor-alpha release in human peripheral blood mononuclear cells. Int J Tissue React 2002; 24: 53–6.

  35. Simonetti P, Gardana C, Pietta P. Caffeic acid as biomarker of red wine intake. Methods Enzymol 2001; 335: 122–30. doi: 10.1016/S0076-6879(01)35237-0

  36. Almeida AA, Farah A, Silva DA, Nunan EA, Gloria MB. Antibacterial activity of coffee extracts and selected coffee chemical compounds against enterobacteria. J Agric Food Chem 2006; 54: 8738–43. doi: 10.1021/jf0617317

  37. Chung MJ, Walker PA, Hogstrand C. Dietary phenolic antioxidants, caffeic acid and Trolox, protect rainbow trout gill cells from nitric oxide-induced apoptosis. Aquat Toxicol 2006; 80: 321–8. doi: 10.1016/j.aquatox.2006.09.009

  38. Rao K, Indap M, Radhika S, Motiwale L. Anticancer activity of phenolic antioxidants against breast cancer cells and a spontaneous mammary tumor. Indian J Pharm Sci 2006; 68: 470–6. doi: 10.4103/0250-474X.27820

  39. Rezaei-Seresht H, Cheshomi H, Falanji F, Movahedi-Motlagh F, Hashemian M, Mireskandari E. Cytotoxic activity of caffeic acid and gallic acid against MCF-7 human breast cancer cells: an in silico and in vitro study. Avicenna J Phytomed 2019; 9: 574–86. doi: 10.22038/AJP.2019.13475

  40. Abera G. Review on high-pressure processing of foods. Cogent Food Agric 2019; 5: 1568725. doi: 10.1080/23311932.2019.1568725

  41. Balakrishna AK, Wazed MA, Farid M. A review on the effect of high pressure processing (HPP) on gelatinization and infusion of nutrients. Molecules 2020; 25: 2369. doi: 10.3390/molecules25102369

  42. Govaris A, Pexara A. Inactivation of foodborne viruses by high-pressure processing (HPP). Foods 2021; 10: 215. doi: 10.3390/foods10020215

Published
2022-01-27
How to Cite
SugaharaY., OhtaT., TaguchiY., HondaS., KashimaY., MatsukawaT., KumazawaS., & KadowakiW. (2022). Resveratrol derivative production by high-pressure treatment: proliferative inhibitory effects on cervical cancer cells. Food & Nutrition Research, 66. https://doi.org/10.29219/fnr.v66.7638
Section
Original Articles